Abstract
Condition-dependence theory predicts that sexual selection will facilitate adaptation by selecting against deleterious mutations that affect the expression of sexually selected traits indirectly via condition. Recent empirical studies have provided support for this prediction; however, their results do not elucidate the relative effects of pre- and postcopulatory sexual selection on deleterious mutations. We used the Drosophila melanogaster model system to discern the relative contributions of pre- and postcopulatory processes to selection against deleterious mutations. To assess second-male ejaculate competition success (P2; measured as the proportion of offspring attributable to the experimental male) and mating success, mutant and wild-type male D. melanogaster were given the opportunity to mate with females that were previously mated to a standard competitor male. This process was repeated for males subjected to a diet quality manipulation to test for effects of environmentally-manipulated condition on P2 and mating success. While none of the tested mutations affected P2, there was a clear effect of condition. Conversely, several of the mutations affected mating success, while condition showed no effect. Our results suggest that precopulatory selection may be more effective than postcopulatory selection at removing deleterious mutations. The opposite result obtained for our diet manipulation points to an interesting discrepancy between environmental and genetic manipulations of condition, which may be explained by the multidimensionality of condition. Establishing whether the various stages of sexual selection affect deleterious mutations differently, and to what extent, remains an important issue to resolve.
Highlights
It is intuitive to think of natural selection as a force operating to remove deleterious mutations from a population, it is perhaps less conventional to think of sexual selection in the same context
Work to date probing the effects of sexual selection on female fitness has focused on sexual selection in toto, and has generated each of neutral [19], negative [20], and positive [21] fitness effects
Studies focusing on total sexual selection on novel deleterious mutations have collectively demonstrated that sexual selection acts to reduce the mutation load [6,7,8]
Summary
It is intuitive to think of natural selection as a force operating to remove deleterious mutations from a population, it is perhaps less conventional to think of sexual selection in the same context. If male siring success is condition-dependent, natural and sexual selection may operate in the same direction on most genes [1]. Several recent studies have demonstrated the efficacy of sexual selection against deleterious mutations [6,7,8], and the potential for sexual selection to reduce mutation load through selection on males [9,10]. These effects may have occurred through precopulatory (e.g., mate choice) or postcopulatory (e.g., ejaculate competition) sexual selection, yet these studies did not attempt to partition total sexual selection amongst the components of siring success. The relative extent to which selection against deleterious mutations occurs through pre- and postcopulatory processes remains unclear
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